A systematic review and meta-analysis of unimodal and multimodal predation risk assessment in birds

Despite a wealth of studies documenting prey responses to perceived predation risk, researchers have only recently begun to consider how prey integrate information from multiple cues in their assessment of risk. We conduct a systematic review and meta-analysis of studies that experimentally manipulated perceived predation risk in birds and evaluate support for three alternative models of cue integration: redundancy/equivalence, enhancement, and antagonism. One key insight from our analysis is that the current theory, generally applied to study cue integration in animals, is incomplete. These theories specify the effects of increasing information level on mean, but not variance, in responses. In contrast, we show that providing multiple complementary cues of predation risk simultaneously does not affect mean response. Instead, as information richness increases, populations appear to assess risk more accurately, resulting in lower among-population variance in response to manipulations of perceived predation risk. We show that this may arise via a statistical process called maximum-likelihood estimation (MLE) integration. Our meta-analysis illustrates how explicit consideration of variance in responses can yield important biological insights.

Figure S1: PRISMA flow chart showing the number of articles discovered and/or retained at each phase of the systematic review.All studies included in the meta-analysis are indicated with asterisks in the References section of the main text, and the list of all studies that were rejected after reading the full text can be found in Supplementary Information Table S3 including the reason for the rejection............. Table S1.Descriptions of trait categories used for coding response variables.When the variable was scored in a way that was inverse to the investment in the trait it measured, the direction of the estimate was corrected by multiplying by -1 (indicated in parentheses following the example description as applicable).For example, inter-scan-interval is inversely related to investment in vigilance, and was therefore multiplied by -1.The predicted effect of an increased perceived predation risk on a category of response variable is indicated in the column "Predicted effect".In order to allow to estimate global effects in our meta-analyses, all variables were coded so that effects in the predicted direction were positive.This means that estimates for categories where the predicted effect was "Decrease" were all multiplied by -1 prior to analysis. .S3: List of studies that were excluded from the meta-analysis based on reading of full text, and their reasons for exclusion. .All studies included in the meta-analysis are indicated with asterisks in the References section of the main text, and the list of all studies that were rejected after reading the full text can be found in Supplementary Information Table S3 including the reason for the rejection.
Table S1.Descriptions of trait categories used for coding response variables.When the variable was scored in a way that was inverse to the investment in the trait it measured, the direction of the estimate was corrected by multiplying by -1 (indicated in parentheses following the example description as applicable).For example, inter-scan-interval is inversely related to investment in vigilance, and was therefore multiplied by -1.The predicted effect of an increased perceived predation risk on a category of response variable is indicated in the column "Predicted effect".In order to allow to estimate global effects in our meta-analyses, all variables were coded so that effects in the predicted direction were positive.This means that estimates for categories where the predicted effect was "Decrease" were all multiplied by -1 prior to analysis.S3: List of studies that were excluded from the meta-analysis based on reading of full text, and their reasons for exclusion.

Reference
Reason for Exclusion Amo, et al. 2 Predator treatment is novel to focal species Amo, et al. 3 Predator treatment is novel to focal species Andreasson, et al. 4 Response variable (Tb) not replicated in other studies Antze and Koper 5 Mobbing calls used were generic response to humans Atkins, et al. 6 Doesn't meet minimum sample size requirements.Level of analysis is "site", with N = 1 treatment and N = 2 control.Aviles, et al. 7 Mixed species level data Berziņš, et al. 8 No control treatment Blackwell, et al. 9 Results do not allow for extraction of effects for each level of treatment separately Breviglieri and Romero 10 Mixed species level data.Cimprich,et al. 11 Season (migration) had insufficient independent studies for inclusion (K = 2) Coslovsky and Richner 12 Not eligible -study of transgenerational effect of predator treatments.Traits investigated in nestlings that were not exposed to cues of predation directly.da Cunha, et al. 13 Mixed species level data Davies and Welbergen 14 Mixed species level data Dutour, et al. 15 Mixed species level data Fardell, et al. 16 Mixed species level data Forsman and Monkkonen 17 Mixed species level data Forsman,et al. 18 Mixed species level data Fransson and Weber 19 Season (migration) had insufficient independent studies for inclusion (K = 2) Ghalambor and Martin 20 Mixed species level data Gomez-Serrano 21 Experimental portion of study used humans as "predator" treatment Griesser 22 for experiments 1: treatment and control observations cannot be compared (different observation durations), for experiment 2: testing information content of calls Griesser 23 No control Groenewoud,et al. 24 No predator treatment Holthuijzen 25 No relevant treatment, assessing if birds recognize heterospecific alarm calls Hua,et al. 26 Mixed species level data Huang,et al. 27 Test of heterospecific information use Hunts,et al. 28 Mixed species level data Ibanez-Alamo, et al. 29 Response type (fecal sac removals) not replicated in any other study.Also, no clear predicted direction of effect based on theory.Iglesias,et al. 30 No control Jones and Sieving 31 Species level data cannot be extracted for control/treatment contrasts Journey,et al. 32 No s.e.(standard error) provided for species level data Keen,et al. 33 Social learning of novel cue Kerman,et al. 34 No control Leavesley and Magrath  No treatment: study tests whether trills convey predator information Macleod,et al. 36 Response variable is cumulative mass gain expressed as percentage (i.e., control and treatment scaled to same range from 0 to 100) Madden,et al. 37 mobbing calls used for treatment were generated in response to humans Martinez,et al. 38 Could not extract species level data-figure resolution too low to extract overlapping data points McIntyre, et al. 39 Effect direction not extractable Morosinotto,et al. 40 response variable = testosterone excluded because no clear predicted effect (authors themselves stated no single prediction) Nilsson and Nord 41 Not relevant -no predator treatment Nocera and Ratcliffe 42 Mixed species level data Pascual and Senar 43 Manipulation is distance to cover Poysa,et al. 44 Not relevant -no predator treatment Rajala, et al. 45 No control Rands and Cuthill 46 manipulation is human threat Roncalli, et al. 47 Response variables not relevant (egg touches, egg rejection) Schneider and Griesser Cannot extract behavioural response to treatments in isolation Serra and Fernandez 49 manipulation is human threat Sieving,et al. 50 Response variables is structure of acoustic response -species specific, not generalizable Thompson,et al. 51 Not relevant -no predator treatment Tilgar and Moks 52 Mixed species level data Tilgar,et al. 53 manipulation is human threat Tolvanen, et al. 54 Not relevant -no predator treatment  Collected to provide more complete meta-data for review and cross checking "predator guild" variable.
Predator guild (bird, mammal, fish, reptile, not specified, or multiple guilds) To allow exploratory analyses of whether specific predator guilds elicit stronger responses than others.

Adult or nest predator
To allow exploratory analyses of whether magnitude of response differs in response to adult versus nest/nestling predators.Setting of the study (field, lab, semi-natural) To allow exploratory analyses of whether magnitude of response differs as a function of study setting.If differences exist, this would have important implications for whether laboratory studies can be extrapolated to field conditions.Treatment (A, O, V, or combination thereof) Key variables of interest to test: 1) whether different modalities of information elicit different response magnitudes consistent with assumption that different modalities provide different degrees of certainty about predation risk, and 2) to evaluate how response to multi-modal cues differ from responses to unimodal cues.Detailed rationale provided in introduction.

Season (breeding, nonbreeding)
To allow exploratory analyses of effect of season (breeding versus nonbreeding).For example, parents may value personal survival differently when Type of comparison (within-or amongsubject) To allow exploratory analyses of whether estimated effect sizes differ for withinversus among-subject designs based on the fact that within-subject designs are generally more powerful because they control for among-subject variability.

Treatment duration (days)
To allow exploratory analyses of effect of treatment duration.Longer treatments may elicit stronger responses for traits that are plastic over longer time scales (e.g., life history traits), but may elicit smaller response for traits that are highly plastic if longer exposure leads to habituation.Control type (blank,  disturbance, nonpredator)   To allow for exploratory analyses of whether control type effects estimated response to manipulations of perceived predation risk.Blank controls compare unmanipulated birds to birds following predator manipulations -and thus do not control for disturbance associated with conducting a treatment."Disturbance" controls employ a matched disturbance (e.g., time that observer is present, presence of novel objects), or "non-predator" controls control for both nonbiological and biological Sex of focal individuals (male, female, both) To allow exploratory analyses of sex-related differences in response magnitude.
Age of focal individuals (A = Adults, N = Nestlings, J = Juveniles, E = Eggs) To allow exploratory analyses of age-related differences in response magnitude.

Figure S1 :
Figure S1: PRISMA flow chart showing the number of articles discovered and/or retained at each phase of the systematic review.All studies included in the meta-analysis are indicated with asterisks in the References section of the main text, and the list of all studies that were rejected after reading the full text can be found in Supplementary Information TableS3including the reason for the rejection.

Table S4 :
List of variables extracted from articles included in the meta-analysis and rationale.